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PNAS 105 (11): 4226-4231

Copyright © 2008 by the National Academy of Sciences.

BIOLOGICAL SCIENCES / EVOLUTION

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

Seth A. Ament*, Miguel Corona{dagger},{ddagger}, Henry S. Pollock{dagger}, and Gene E. Robinson*,{dagger},§,¶

*Neuroscience Program, {dagger}Department of Entomology, and §Institute for Genomic Biology, University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801

Contributed by Gene E. Robinson, January 22, 2008

Received for publication December 20, 2007.

Abstract: It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes. Age-related division of labor in honey bee colonies, a highly derived behavioral system, involves the performance of different feeding-related tasks by different groups of individuals. Older bees acquire the colony's food by foraging for nectar and pollen, and the younger "nurse" bees feed larvae processed foods. The transition from hive work to foraging has been shown to be socially regulated and associated both with decreases in abdominal lipid stores and with increases in brain expression of genes implicated in feeding behavior in Drosophila melanogaster. Here we show that division of labor is influenced by a canonical regulator of food intake and energy balance in solitary species, the insulin/insulin-like growth factor signaling (IIS) pathway. Foragers had higher levels of IIS gene expression in the brain and abdomen than did nurses, despite their low lipid stores. These differences are likely nutritionally mediated because manipulations that induced low lipid stores in young bees also up-regulated these genes. Changes in IIS also causally influenced the timing of behavioral maturation: inhibition of the insulin-related target of rapamycin pathway delayed the onset of foraging in a seasonally dependent manner. In addition, pathway analyses of microarray data revealed that nurses and foragers differ in brain energy metabolism gene expression, but the differences are opposite predictions based on their insulin-signaling status. These results suggest that changes in the regulation of the IIS pathway are associated with social behavior.

Key Words: Apis mellifera • behavioral maturation • social insect • nutrition • foraging

Freely available online through the PNAS open access option.

Author contributions: S.A.A., M.C., and G.E.R. designed research; S.A.A., M.C., and H.S.P. performed research; S.A.A. and M.C. analyzed data; and S.A.A., M.C., and G.E.R. wrote the paper.

{ddagger}Present address: Department of Ecology and Evolution, University of Lausanne, Quartier-UNIL-Sorge, Bâtiment Biophore Bureau 3211, CH-1015 Lausanne, Switzerland.

The authors declare no conflict of interest.

This article contains supporting information online at www.pnas.org/cgi/content/full/0800630105/DC1.

To whom correspondence should be addressed. E-mail: generobi{at}life.uiuc.edu

© 2008 by The National Academy of Sciences of the USA

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